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Proposal of Glycocaulis Abyssi Gen. Nov., Sp. Nov., Belonging to the Family Hyphomonadaceae

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Proposal of Glycocaulis Abyssi Gen. Nov., Sp. Nov., Belonging to the Family Hyphomonadaceae International Journal of Systematic and Evolutionary Microbiology (2013), 63, 2207–2215 DOI 10.1099/ijs.0.047894-0 Cauliform bacteria lacking phospholipids from an abyssal hydrothermal vent: proposal of Glycocaulis abyssi gen. nov., sp. nov., belonging to the family Hyphomonadaceae Wolf-Rainer Abraham,1 Heinrich Lu¨nsdorf,1 Marc Vancanneyt2 and John Smit3 Correspondence 1Helmholtz Center for Infection Research, Inhoffenstrasse 7, D-38124 Braunschweig, Germany Wolf-Rainer Abraham 2Laboratorium voor Microbiologie, Universiteit Gent, Belgium wolf-rainer.abraham@helmholtz- 3 hzi.de Department of Microbiology and Immunology, University of British Columbia, Vancouver, British Columbia, Canada Cauliform bacteria are prosthecate bacteria often specialized for oligotrophic environments. A polyphasic approach, comprising 16S rRNA gene sequencing, lipid analysis and salt tolerance characterizations, was used to clarify the taxonomy of one isolate, strain MCS 33T, obtained from above the hot water plume of a deep-sea hydrothermal vent near Vancouver island, Canada. Cells contained no detectable phospholipids or sulpholipids, but did contain 1,2-di-O-acyl-3-O-a-D- glucopyranosylglycerol, 1,2-di-O-acyl-3-O-a-D-glucopyranuronosylglycerol and the novel lipid 1,2-di-O-acyl-3-[O-a-D-glucopyranuronosyl]glycerol-69-N-glycine. It is assumed that the various glucoronosyl lipids are replacing, at least partially, the phospholipids in their various tasks in the cell cycle. The G+C content of the genomic DNA of strain MCS 33T was 62.8 mol%, and Q10 was the predominant respiratory ubiquinone. The 16S rRNA gene sequence of this chemoheterotrophic, aerobic, moderately halophilic strain showed only a low similarity of 94.4 % to that of Oceanicaulis alexandrii C116-18T, and both strains also differed based on their lipids. Although the novel strain was isolated from seawater sampled near a hydrothermal vent, its optimum temperature for growth was 30 6C. The main cellular fatty acids were C18 : 1v7c,C18 : 0 and the unknown fatty acid ECL 11.798, and the main hydroxy fatty acid was C12 : 0 3-OH. The strain is proposed to represent a novel species of a new genus, Glycocaulis abyssi gen. nov., sp. nov. The type strain of the type species is MCS 33T (5LMG 27140T5CCUG 62981T). For decades bacteria having a stalk and reproducing with this is that these bacteria exhibit the physiological regularly by the separation of two cells that are morpho- properties of oligotrophs (Poindexter, 1981). Henrici and logically and behaviourally different from each other were Johnson (1935) placed bacteria possessing these character- regarded as members of the genus Caulobacter (Poindexter istics into the new genus Caulobacter. Stahl et al. (1992) 1964). One descendant is non-motile, sessile due to analysed the phylogeny of a number of caulobacteria and adhesion to the substratum and prosthecate, possessing a found low levels of similarity between sequences of the 16S tubular appendage of variable length – a prostheca (Staley rRNA gene. We analysed a large number of strains for their 1968). The other descendant is actively motile by means of pattern of proteins, polar lipids and 16S rRNA gene one polar flagellum. The mode of reproduction of the sequences (Abraham et al., 1997) and revealed the dimorphic prosthecate bacteria is regarded as a reflection paraphyletic nature of marine caulobacteria belonging of an ecological adaptation helping to disperse the mainly to the two genera Brevundimonas (Segers et al., population at each generation and thereby minimizing 1994) and Maricaulis (Abraham et al., 1999). The marine competition between descendants for resources. Consistent isolates show particularly high diversity, with strains differing so much from the genus Maricaulis that they Abbreviation: FAME, fatty acid methyl ester. cannot be included in this genus but belong to separate The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene genera, i.e. Oceanicaulis (Stro¨mpl et al., 2003) and sequence of strain MCS 33T is AJ227811. Woodsholea (Abraham et al., 2004). We describe here T Three supplementary figures are available with the online version of this another of these isolates, MCS 33 , which does not fit in paper. any of the described genera. 047894 G 2013 IUMS Printed in Great Britain 2207 W.-R. Abraham and others The strains used in this study were obtained from the American type Culture Collection (ATCC), the Deutsche Sammlung fu¨r Mikroorganismen und Zellkulturen (DSMZ), the Department of Microbiology and Immunology at the University of British Columbia (MCS strains, Maricaulis virginensis VC-5T, Woodsholea maritima CM243T) and from C. Stro¨mpl, Helmholtz Center for Infection Research, Braunschweig, Germany (Oceanicaulis alexandrii C116- 18T). The strains were grown in the marine medium SPYEM: 30 g sea salts (Sigma), 0.5 g NH4Cl, 1 litre MilliQ-water. After autoclaving and cooling to ambient temperature, 20 ml 506PYE, 2 ml 50 % glucose (sterile) and 5 ml riboflavin (0.2 mg ml21) sterile filtered were added. 506PYE includes 100 g peptone and 50 g yeast extract in 1 litre deionized water (autoclaved). The strains were grown in 2-litre Erlenmeyer flasks at 30 uC and 100 r.p.m. and the biomass was harvested in the late exponential phase after 72 h. For electron microscopy, growing cells were prepared for negative staining, embedding and ultrathin sectioning as described in detail by Yakimov et al. (1998). Cells of strain MCS 33T showed morphological features typical of caulobacteria, when analysed by transmission electron microscopy. During cell division two morphotypes of daughter cells were observed: first, the swarmer cell, which is monopolarly and monotrichously flagellated; and, T Fig. 1. Ultrastructure of cells of strain MCS 33 . (a) Negatively second, the prosthecate daughter cell with its stalk stained dividing cells, which show characteristic caulobacterial (diameter 85 nm), ending in a spherical holdfast (diameter T features. One daughter cell is the swarmer cell and carries a single 140 nm) (Fig. 1a). Typically, strain MCS 33 formed flagellum. It is still connected to the second prosthecate daughter groups or clusters of cells (Fig. 1b), often bundled by cell by an extended septum. The stalk is terminated by a aggregated holdfasts (Fig. 1c, circle). Overall cell shape was characteristic spherical holdfast. (b) Survey view of a cluster of vibrioid and cell length ranged from 1.3 to 2.5 mm and cell cells, which show prostheca of different developmental states. (c) width from 0.65 to 0.72 mm. The interior part of the stalk Ultrathin section. A longitudinal cut shows the vibrioid shape of the appeared only slightly electron-dense and was surrounded cell body, which contains a pronounced chromosome, surrounded by the electron-translucent periplasm. The cell-wall by densely packed cytoplasm. Many prostheca end up in a tight architecture was Gram-negative; an outer membrane, cluster of holdfasts and form a typical rosette-like ensemble (white which was intensely undulated, formed the outer boundary circle). (d) Detailed view of the cell wall, showing the outer of the cell (Fig. 1c, d). membrane and cytoplasmic membrane. The periplasm appears as an electron-translucent matrix. fl, Flagellum; es, extended septum; Genomic DNA was isolated from two loopfuls of bacterial pr, prosthecum; hf, holdfast; cp, cytoplasm; om, outer membrane; cells using the DNeasy Blood and Tissue kit for purification cm, cytoplasmic membrane; stars, chromosome. Bars 1 mm (a, b), of total DNA (Qiagen) with the addition of RNase A 500 nm (c), 50 nm (d). (Sigma), according to the manufacturers’ instructions. DNA was enzymically digested as described by Gehrke et al. (1984) and the mean G+C content was determined by bootstrap consensus tree using the neighbour-joining HPLC (Tamaoka & Komagata, 1984). Calculations were algorithm (Fig. 2), maximum-parsimony (Fig. S1, available carried out according to Mesbah et al., (1989), with non- in IJSEM Online) and maximum linkage (Fig. S2) with methylated lambda-phage DNA (Sigma) as a standard. MEGA version 5.0.5 (Tamura et al., 2011), based on 1000 Amplification of the 16S rRNA gene and sequencing was resamplings and with Caulobacter vibrioides VKM1496T as done as described previously (Abraham et al., 2010). The an outgroup. phylogenetic position of strain MCS 33T was determined by analysis of the 16S rRNA gene sequence (Abraham et al., Isoprenoid quinones were extracted with chloroform/ 1999) using the software CLUSTAL W (Thompson et al., methanol (2 : 1, v/v) and analysed by the method published 1997). The 16S rRNA gene sequence showed 94.2 % by Minnikin et al. (1984). The main ubiquinone of strain similarity to that of both Maricaulis maris ATCC 15268T MCS33T was ubiquinone Q-10. For whole-cell fatty acid and O. alexandrii C116-18T and 93.5 % to W. maritima analysis, cells were saponified [15 % (w/v) NaOH, 30 min, CM243T. Alignment of sequences from the EMBL database 100 uC], methylated to fatty acid methyl esters (FAMEs) (Karsch-Mizrachi et al., 2012) was used to construct a (methanolic HCl, 10 min, 80 uC) and extracted [hexane/ 2208 International Journal of Systematic and Evolutionary Microbiology 63 Glycocaulis abyssi gen. nov., sp. nov. T Hyphomonas rosenbergii VP6 (AF082795) T 89 Hyphomonas hirschiana VP5 (AF082794) 100 T 0.01 Hyphomonas neptunium LE670 (AF082798) T 51 Hyphomonas polymorpha DSM 2665 (AJ227813) T Hyphomonas adhaerens MHS-3 (AF082790) 100 T 100 Hyphomonas jannaschiana VP2 (AJ227814) T Hyphomonas oceanitis SCH89 (AF082797) 97 T 92
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